Venomous Noodles: The Evolution of Toxins in Nemertea through Positive Selection and Gene Duplication

Abstract

Some, probably most and perhaps all, members of the phylum Nemertea are poisonous, documented so far from marine and benthic specimens. Although the toxicity of these animals has been long known, systematic studies on the characterization of toxins, mechanisms of toxicity, and toxin evolution for this group are scarce. Here, we present the first investigation of the molecular evolution of toxins in Nemertea. Using a proteo-transcriptomic approach, we described toxins in the body and poisonous mucus of the pilidiophoran Lineus sanguineus and the hoplonemertean Nemertopsis pamelaroeae. Using these new and publicly available transcriptomes, we investigated the molecular evolution of six selected toxin gene families. In addition, we also characterized in silico the toxin genes found in the interstitial hoplonemertean, Ototyphlonemertes erneba, a meiofaunal taxa. We successfully identified over 200 toxin transcripts in each of these species. Evidence of positive selection and gene duplication was observed in all investigated toxin genes. We hypothesized that the increased rates of gene duplications observed for Pilidiophora could be involved with the expansion of toxin genes. Studies concerning the natural history of Nemertea are still needed to understand the evolution of their toxins. Nevertheless, our results show evolutionary mechanisms similar to other venomous groups.

New Pyridyl and Dihydroisoquinoline Alkaloids Isolated from the Chevron Nemertean Amphiporus angulatus

“…Several papers have been published in recent years reporting transcriptomic investigations into various nemerteans [36][37][38][39]. These investigations only searched for peptidic toxins.…”

“…The biosynthesis of nemertelline and its congeners seems very likely to result from a hetero-dimerization of anabaseine (providing the A and B rings of nemertelline) with an activated precursor of isoanatabine (providing the C and D rings of the tetrapyridyl, as shown in Figure 9). The postulated 3′ -methyl-nemertelline and 3′ -hydroxynemertelline (see Figure 1 Several papers have been published in recent years reporting transcriptomic investigations into various nemerteans [36][37][38][39]. These investigations only searched for peptidic toxins.…”